Published online before print December 19, 2006, 10.1148/radiol.2422060030
(Radiology 2006;242:573.)
A more recent version of this article appeared on December 1, 2006
© RSNA, 2006
Bronchial Measurement with Three-dimensional Quantitative Thin-Section CT in Patients with Cystic Fibrosis1
Michel Montaudon, MD, PhD,
Patrick Berger, MD, PhD,
Agathe Cangini-Sacher, MD,
Gabriel de Dietrich, PhD,
José Manuel Tunon-de-Lara, MD, PhD,
Roger Marthan, MD, PhD and
François Laurent, MD
1 From the Laboratory of Cellular Respiratory Physiology, Université Bordeaux 2, Bordeaux, France, and Institut National de la Santé et de la Recherche Médicale, E 356, F 33076, Bordeaux, France (M.M., P.B., J.M.T.d.L., R.M., F.L.); Department of Thoracic and Cardiovascular Imaging, CHU de Bordeaux, Hôpital du Haut-Lévêque, F 33604, Hôpital Cardiologique, avenue de Magellan, 33604 Pessac, France (M.M., A.C., F.L.); and Université Bordeaux 1, Talence, France (G.d.D.). Received January 6, 2006; revision requested March 7; revision received March 31; accepted May 3; final version accepted July 5. Supported by grants from Programme Hospitalier de Recherche Clinique in 2002.
Address correspondence to F.L. (e-mail: francois.laurent{at}chu-bordeaux.fr).
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ABSTRACT
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Purpose: To prospectively compare bronchial measurements obtained with three-dimensional quantitative thin-section computed tomography (CT) with those obtained with thin-section CT scores in the assessment of the severity of pulmonary cystic fibrosis (CF).
Materials and Methods: Ethics committee approval was obtained. Sixteen patients with CF (mean age, 26.6 years; range, 18–42 years) and five healthy volunteers (mean age, 27.4 years; range, 21–44 years) gave written informed consent, underwent multi–detector row CT and a pulmonary function test (PFT), and were divided into three groups: group A, healthy volunteers; group B, patients with mild CF (forced expiratory volume in 1 second [FEV1] > 80%); and group C, patients with severe CF (FEV1 < 80%). Two observers obtained thin-section CT scores with eight scoring systems. Bronchial cross-sectional wall area (WA), lumen area (LA), airway area, and wall thickness (WT) were measured with customized software and were normalized on the basis of subject body surface. Morphologic characteristics, PFT results, thin-section CT scores, and quantitative measurements were compared among the three groups with analysis of variance. Correlations among bronchial measurements, PFT results, and CT scores were calculated with the Spearman correlation coefficient.
Results: Thin-section CT scores were different between group C and either group A or group B (P < .05). WA and WT were significantly different among all groups (P < .05). Interscore correlations and correlations between bronchial parameters and scores were high (r > 0.89, P < .0001). Scores, WA, and WT were significantly correlated with PFT obstructive indexes (P < .047).
Conclusion: WA and WT assessed with dedicated software on multi–detector row CT images allow evaluation of the severity of pulmonary CF.
© RSNA, 2006
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INTRODUCTION
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Lung function abnormalities in patients with cystic fibrosis (CF) are related to structural abnormalities, including loss of respiratory epithelium. These abnormalities affect smooth muscle tone, cause extensive inflammation of the bronchial wall (thus leading to thickened cartilaginous airways), and result in loss of cartilage volume (1). So far, detection and quantification of these structural changes have been based mainly on histologic findings, but noninvasive methods are needed to evaluate changes in the airways. In addition, evaluation of lung damage at the time of diagnosis is important to initiate appropriate treatment, delay disease progression, and assess the effectiveness of new therapies. Assessment of lung disease is currently performed with a pulmonary function test (PFT), although the sensitivity of this test for the detection of early damage is low and weakly correlated with morphologic abnormalities (2–5).
The better sensitivity of computed tomography (CT) in the detection of lung damage beyond that of chest radiography has long been recognized (2,3). Further evaluation has revealed correlation between CT scores and other clinical findings (6,7) and between CT scores and response to treatment, leading one author to propose CT as an outcome surrogate for research studies (8). Regarding scores, de Jong et al (9) evaluated five scoring systems for quantification of CT findings and found that scoring systems were reproducible and correlated with PFT. The feasibility of three-dimensional quantification of bronchial parameters at multi–detector row CT with dedicated software has been demonstrated (10). In addition, accurate and reproducible measurement of lumen area (LA) and wall area (WA) of bronchi on thin-section CT images has been achieved (11). However, conflicting results have been reported when bronchial dimensions measured with thin-section CT were considered (12–14).
Thus, the purpose of our study was to prospectively compare bronchial measurements obtained with three-dimensional quantitative thin-section CT with those obtained with thin-section CT scores in the assessment of the severity of pulmonary CF.
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MATERIALS AND METHODS
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Study Groups
All participants gave written informed consent for our study, which was approved by the ethical committee at our institution. Sixteen consecutive nonsmokers with CF (six men, 10 women; mean age, 26.6 years; range, 18–42 years) were included in this study from June 2003 up to October 2004. A control group of five healthy volunteers (four men, one woman; mean age, 27.4 years; range, 21–44 years) without a history of respiratory disease and with normal PFT results was included for comparison. All patients were followed up in our institution, where annual PFT and biennial CT are part of the routine examination protocol in young adults with CF. CF was diagnosed with a positive sweat test, the presence of a genotype for known CF mutations, an abnormal potential difference measured across the nasal mucosa, or any combination of these findings.
In patients with CF, CT was performed under stable conditions in the absence of any acute event for at least 3 weeks prior to the evaluation. Subjects were divided into three groups according to the PFT results: healthy volunteers (group A, n = 5), patients with mildly severe CF (group B, n = 6), and patients with severe CF (group C, n = 10). Severe CF was defined as forced expiratory volume in 1 second (FEV1) of less than 80% of the predicted value, whereas mild CF was defined as FEV1 of more than 80% of the predicted value.
Thin-Section CT
Volumetric acquisition of the whole lungs was performed at full inspiration with a 16-section multi–detector row CT scanner (Somatom Sensation 16; Siemens, Erlangen, Germany) and the following parameters: 120 kV, 33 mAs, and 0.75-mm native section thickness. Images were reconstructed in the transverse plane with 1-mm reconstruction thickness, 300–380-mm2 field of view, and 1-mm reconstruction interval. Additional 1-mm-thick thin-section CT scans were obtained every 2 cm at full expiration.
Scoring Systems and Evaluation
We selected eight thin-section scoring systems for evaluation (2–5,7,15–17). All scores were assigned in a semiquantitative manner to a subset of patients with the following abnormalities: (a) bronchiectasis, (b) peribronchial thickening, (c) mucus plugging, (d) sacculations or abscesses, (e) bullae, (f) emphysema, (g) air trapping or hyperinflation, (h) collapse or consolidation, (i) mosaic perfusion or ground-glass opacities, (j) acinar nodules or alveolar consolidation, and (k) thickening of intra- and interlobular septa. Two observers with 10 (M.M.) and 15 (F.L.) years of experience in chest CT assigned scores to thin-section CT scans. After a consensus for standardizing the scoring methods was reached, all 21 scans were assigned scores in random order; the observers were independent and blinded to patients' characteristics.
Bronchial Dimensions
An independent observer with 5 years experience in chest CT (A.C.) measured bronchial dimensions on CT scans with dedicated software, as described previously (10). Briefly, we measured WA and LA for each patient and each bronchial generation. We calculated cross-sectional area of the airway by summing WA and LA. We also calculated wall thickness (WT) as follows: WT = 
[(WA + LA)/
] – (LA/). Measurements were obtained considering, on one hand, all assessable bronchi and, on the other hand, only nondilated bronchi (those bronchi with a ratio of less than 0.88 between the LA of the bronchi and the surface of its accompanying artery) (18). One measurement was obtained per bronchus. The software provided fully automated segmentation of the skeleton (ie, airway central axis of the bronchial tree), and two-dimensional reformatted images strictly perpendicular to the central axis were automatically obtained. The rest of the procedure was semiautomatic: The observer chose the bronchus and determined the bronchial generation and reformatted cross section on which measurements were to be obtained (10). The precise location where a measurement was obtained was determined by the observer in order to have the minimal percentage of bronchial cross section circumference in contact with a pulmonary artery section. Bronchi were excluded when no reformatted section could be used for measurement purposes because of motion artifacts.
Analysis was limited to the third through sixth generations because the number of detected bronchi was low after the sixth generation and because comparison with the artery surface could not be performed within the hili.
PFT Results
The PFT results were obtained with body plethysmography (Jaëger; Masterlab, Geispolsheim-Gare, France). PFT was performed before multi–detector row CT, with a mean interval between examinations of 4 days (range, 0–25 days; median, 1 day).
Statistical Analysis
One-way analysis of variance was used to compare morphologic characteristics and PFT results among the three groups; comparisons between groups were assessed with the Tukey-Kramer multiple-comparison test.
Correlations between scores calculated for each patient and PFT results were assessed with the Spearman rank correlation coefficient. Scores among groups were compared with the Kruskal-Wallis test; differences between groups were compared with a multiple-comparison Kruskal-Wallis Z test with Bonferroni correction. Log transformation was not performed, since many scores were zero.
WA, LA, cross-sectional area of the airway, and WT did not follow a normal distribution, even after transformation. Therefore, we used original data for comparison. Bronchial measurements were normalized with the subject's body surface (19) and compared among the three groups by using repeated analysis of variance, with subject group serving as the between-subjects factor and bronchial generation serving as the within-subjects factor. The Tukey-Kramer multiple-comparison test was used to compare subject groups.
Correlations between bronchial measurements and PFT indexes on one hand and bronchial measurements and scores on the other hand were calculated with Spearman rank correlation coefficients.
Results were considered statistically significant when P values were less than .05. All analyses were performed with NCSS 2001 software (NCSS Statistical Software, Kaysville, Utah) by an independent observer (P.B.).
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RESULTS
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Study Groups and PFTs
There was a significant difference in weight and height between the groups (one-way analysis of variance, P < .0001 and P = .019, respectively; Table 1). With use of multiple-comparison tests, this difference existed only for weight and body surface between groups A and C because of the slower growth rate of patients with severe CF. No difference was found between groups A and B or between groups B and C. Thus, we corrected bronchial dimensions by using body surface to avoid the potential bias due to differences in weight between patient groups.
All functional parameters except total lung capacity were significantly different among all groups (P 
.43, one-way analysis of variance; Table 1). However, using multiple-comparison tests, differences existed between groups A and C on one hand and between groups B and C on the other hand when considering FEV1, forced vital capacity (FVC), and forced expiratory flow between 25% and 75% of vital capacity (FEF25–75). FEV1 and FVC were different between only groups A and C. No difference was found when considering residual volume and specific airway conductance.
Thin-Section CT Scores
Abnormal findings were reported in two healthy volunteers: Both readers reported a linear opacity in the middle lobe in one volunteer; observer 2 reported mild dilated bronchi in both lower lobes in the other volunteer. In patients with CF, thickened bronchial walls were observed in 16 patients (94%) by observer 1 and in 17 patients (100%) by observer 2; bronchiectasis was observed in 15 patients (88%) by observer 1 and in 16 patients (94%) by observer 2; mucoid impactions were observed in 15 patients (88%) by both observers; consolidations and alveolar nodules were observed in six patients (35%) by observer 1 and in 14 patients (82%) by observer 2; atelectasis was observed in five patients (29%) by observer 1 and in 14 patients (82%) by observer 2; mosaic attenuation was observed in nine patients (53%) by observer 1 and in 10 patients (59%) by observer 2; parenchymal distention was observed in nine patients (53%) by both observers; air trapping was observed in eight patients (67%) by observer 1 and in nine patients (75%) by observer 2; ground-glass opacity was observed in one patient (6%) by observer 1 and in seven patients (42%) by observer 2; septal lines were observed in six patients (35%) by observer 1 and in 13 patients (76%) by observer 2.
Thin-section CT scores (Table 2) were significantly different among the three groups (P < .002, Kruskal-Wallis test). However, when the multiple-comparison Z test with Bonferroni correction was used, a significant difference was found for all scores, with the exception of the studies of Dorlochter et al (16) and Santamaria et al (17), between groups A and C (P < .05) but not between groups B and C or groups A and B. No difference was found between groups when considering scores obtained by Dorlochter et al (16) or Santamaria et al (17).
Interobserver correlations for each score and for interscore correlations were high (r > 0.9 and r > 0.89, respectively; P < .0001). Scores were inversely correlated to FEV1, FVC, FEV1/FVC ratio, FEF25–75, and specific airway conductance (|r| 
0.54, P < .05) but not to total lung capacity when scores obtained in the studies of Bhalla et al (2), Maffessanti et al (3), Stiglbauer et al (4), Helbich et al (5), and Nathanson et al (15) were considered. Scores were not correlated with total lung capacity.
Bronchial Wall Parameters
Significant differences among groups (Figs 1–3, Table 3) were found, regardless of the bronchial parameter considered (P < .001, Kruskal-Wallis test) (Table 4). When comparing each pair of groups for each parameter with the Tukey-Kramer test, groups were differentiated when considering WT (Fig 4). Significant differences were found (a) between groups A and C on one hand and between groups B and C on the other hand when considering WA (Fig 4) and cross-sectional area of the airway and (b) between groups A and C when comparing LA. These results were not different when considering all measured bronchi or only nondilated airways.
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Figure 1: Representative CT scans obtained in healthy volunteers (group A). A, Native transverse thin-section CT image; B, frontal view of binary volume and skeleton; and reformatted images orthogonal to the main bronchus axis, C, before, and, D, after segmentation. The analyzed bronchus is indicated by the arrow in A and by the arrowhead in B.
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Figure 2: Representative CT scans obtained in patients with mild CF (group B). A, Native transverse thin-section CT image; B, frontal view of binary volume and skeleton; and reformatted images orthogonal to the main bronchus axis, C, before, and, D, after segmentation. The analyzed bronchus is indicated by the arrow in A and by the arrowhead in B.
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Figure 3: Representative CT scans obtained in patients with severe CF (group C). A, Native transverse thin-section CT image; B, frontal view of binary volume and skeleton; and reformatted images orthogonal to the main bronchus axis, C, before, and, D, after segmentation. The analyzed bronchus is indicated by the arrow in A and by the arrowhead in B.
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WA, cross-sectional area of the airway, and WT were significantly correlated with all scores when all assessable bronchi or only nondilated bronchi were considered (Table 5). WA and WT were significantly correlated with all functional indexes except total lung capacity when all assessable bronchi or only nondilated bronchi were considered (Table 6).
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DISCUSSION
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The results of our study indicate that CT measurement of bronchial WT and WA with dedicated software, as compared with CT scoring systems, allows better discrimination of patients with CF from healthy subjects and better assessment of the severity of airway abnormalities.
Since CT is an established method used to assess airway damage in patients with CF, thin-section CT scoring systems have frequently been used to quantify airway abnormalities (2,3,5–9,12,13,15–17,20–27). All of these scoring systems rely on composite scores to enable subjective estimation of features on CT scans. A strong correlation between the FEV1 value and the thin-section CT scoring system has been reported (5,9,15,23). In young children with mild to moderate lung disease, a broad range of pulmonary abnormalities can be found despite normal PFT results (4,22). Additionally, thin-section CT scoring systems may be more sensitive than the PFT in the detection of disease progression in patients with CF (9).
In our study, CT scores were correlated with PFT results, especially those reflecting bronchial obstruction (ie, FEV1, FEF25–75, FEV1/FVC ratio, and specific airway conductance). Each scoring system was correlated with the other systems. The present results are in agreement with those of de Jong et al (9), who observed good intra- and interobserver reproducibility, which indicated that scores were reliable and reproducible. In our study, the population was divided into two groups according to FEV1 values. CT scores were significantly different between the three groups (one-way analysis of variance). However, when comparing pairs of groups (Kruskal-Wallis Z test with Bonferroni correction), a significant difference was observed only between healthy subjects and patients with severe CF. In addition, increased variability has been observed when the scores were low (9). Early detection of CF therefore requires sufficient resolution at the lower end of the scoring system scale. Another limitation of scoring systems is the intra- and interobserver variation of the recognition of CT abnormalities despite good inter- and intraobserver reproducibility of scores themselves (9). These observations suggest that CT scores may reveal limitations when early detection and follow-up of the early progression of CF are considered. In addition, in our study, CT scores did not indicate a significant difference between mild (group B) and severe (group C) CF.
In our study, we used customized dedicated and validated software to detect internal and external contours of bronchi (10). Although the method is automated, it allows correction of the airway external wall contour despite its connection to a vessel, without assuming a perfect roundness and symmetry of the WA. The accuracy of the inner and outer wall two-dimensional segmentation of a bronchus has been previously validated in experimental studies (11). The present software also assesses the bronchial generation and therefore determines the involvement of each bronchial generation in the airway changes. The difference in WA and WT between groups of patients with CF who have different functional impairment was greater when fourth to sixth generation bronchi were considered.
Airway WT and LA due to bronchiectasis are expected to be greater in patients with CF than in control subjects because of inflammatory changes and bronchial dilatation. Increased thickening of WA in patients with CF was found in our study and in other clinical studies (13,14). This may be secondary to structural changes per se or mucosal secretions lining the lumen side of the airway or, more likely, to both phenomena. Because of the lack of a difference in attenuation between the mucosa and the muscular wall, no CT study can be used to discriminate between these two mechanisms.
The results concerning LA deserve further discussion. LA measurements were significantly larger in the group of patients with severe CF than in the group of control subjects. Other studies have shown similar findings (13) or conversely decreased LA (14). These discrepancies between studies may be related to various stages of CF-related airway disease in life, as well as to methodologic differences. In our study, young adults were included, whereas young children (average age, 2.4 and 1.3 years, respectively) were recruited in the studies by Long et al (13) and Martinez et al (14). In addition, the dilatation of airway lumen in infants with CF increased significantly with age (13). In a longitudinal study in which CT and PFT were performed at baseline and after a 2-year interval, airway WT increased without a concomitant increase in LA and there was a correlation between the increase in airway WT and the decrease in FEF25–75 (12). Finally, WA and WT appear to be the most informative indexes for evaluation of airway changes in patients with CF.
Some limitations in our study require further discussion. Important challenges in measuring airway dimensions in patients with CF are lung growth and the difficulty in identifying airways on subsequent scans because of mucus plugging. Despite the fact that our software theoretically allows us to select the same airway and to measure the airway dimensions at the same section level, our patients did not undergo CT twice. Therefore, the contribution of the present software to the comparison between two CT studies cannot be evaluated when morphologic changes occur. In addition, airway lumen varies as a function of lung volume, and this effect may be even more prominent when airway compliance is abnormal. This is why spirometric gating has been proposed to examine the lung at the same volume of inflation (14).
Since we intended to keep multi–detector row CT acquisition within the standards of routine imaging, we did not use respiratory gating in our study. However, all examinations were performed in subjects at full inspiration, a respiratory status that is less affected by airway dimension variability (28). Another limitation of the use of CT to assess airway changes in patients with CF is the risk of radiation exposure, which remains a concern, particularly when young children are examined. In addition, the number of patients included in this study was relatively small and there was a marked difference between PFT results in patients with severe CF and PFT results in patients with mild CF. This difference likely enhanced differences in airway parameters and correlation with physiologic variables. Nevertheless, differences were also observed between the patients with mild CF and the healthy control subjects; this was the major finding of our study.
In conclusion, WA and WT as assessed with dedicated software on thin-section multi–detector row CT images are valuable indexes for determining the severity of airway impairment in patients with CF.
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ADVANCE IN KNOWLEDGE
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- Measurement of bronchial wall thickness and wall area on three-dimensional quantitative thin-section CT scans with dedicated software, as compared with CT scoring systems, allows better assessment of the severity of airway abnormalities in patients with cystic fibrosis.
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FOOTNOTES
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Abbreviations: CF = cystic fibrosis • FEF25–75 = forced expiratory flow between 25% and 75% of vital capacity • FEV1 = forced expiratory volume in 1 second • FVC = forced vital capacity • LA = lumen area • PFT = pulmonary function test • WA = wall area • WT = wall thickness
Author contributions: Guarantors of integrity of entire study, P.B., F.L.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, M.M., P.B., A.C., F.L.; clinical studies, M.M., G.d.D., F.L.; statistical analysis, P.B., R.M.; and manuscript editing, M.M., P.B., J.M.T.d.L., R.M., F.L.
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M. Montaudon, P. Berger, G. de Dietrich, A. Braquelaire, R. Marthan, J. M. Tunon-de-Lara, and F. Laurent
Assessment of Airways with Three-dimensional Quantitative Thin-Section CT: In Vitro and in Vivo Validation
Radiology,
December 1, 2006;
242(2):
563 - 572.
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ABSTRACT
INTRODUCTION
= group A, 
= group B, and 
= group C). Log-transformed data of mean WT (A and C) and mean WA (B and D) in each group are plotted against bronchial generations. Measurements were obtained for all assessable bronchi on one hand and for nondilated bronchi on the other hand. Error bars represent the standard error of the mean for each group at each bronchial generation. WA was different between groups A and B and between groups A and C. WT was different between all pairs of groups.